Soluble human IL-1 receptor type 2 inhibits ectopic endometrial tissue implantation and growth: Identification of a novel potential target for endometriosis treatment

American Journal of Pathology

Volumn 181, Issue 4, 2012, Pages 1197-1205

  Khoufache, Khaled ^a   Bondza, Patrick Kibangou ^a   Harir, Noria ^a   Daris, Marleen ^b   Leboeuf, Mathieu ^b   Mailloux, Jacques ^b   Lemyre, Madeleine ^b   Foster, Warren ^c   Akoum, Ali ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

^c MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA3 INTEGRIN; CD51 ANTIGEN; GELATINASE A; GELATINASE B; INTERLEUKIN 1 RECEPTOR TYPE II; PROTEIN BCL 2; SOLUBLE INTERLEUKIN 1 RECEPTOR TYPE II; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; UNCLASSIFIED DRUG; VASCULOTROPIN;

ADULT; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENDOMETRIOSIS; ENZYME INDUCTION; FEMALE; GROWTH INHIBITION; HUMAN; HUMAN TISSUE; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE GROWTH; TISSUE SURVIVAL;

ADULT; ANGIOGENESIS INDUCING AGENTS; ANIMALS; BIOPSY; BODY WEIGHT; CELL ADHESION; CELL MOVEMENT; ENDOMETRIOSIS; ENDOMETRIUM; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MICE; MICE, NUDE; MOLECULAR TARGETED THERAPY; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, INTERLEUKIN-1 TYPE II; RNA, MESSENGER; SOLUBILITY; STAINING AND LABELING; SURVIVAL ANALYSIS;

EID: 84866523766     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.06.022     Document Type: Article

References (64)

1. L.C. Giudice Clinical practice Endometriosis N Engl J Med 362 2010 2389 2398
2. K.J. Holoch, B.A. Lessey Endometriosis and infertility Clin Obstet Gynecol 53 2010 429 438
3. D. Cramer, E. Wilson, F. Stillman, M. Berger, S. Belisle, I. Schiff, B. Albrechts, M. Gibsin, B. Stadel, S. Shoenbaum The relation of endometriosis to menstrual characteristics smoking and exercice JAMA 255 1986 1904 1908 (Pubitemid 16167462)
4. J.N. Painter, C.A. Anderson, D.R. Nyholt, S. Macgregor, J. Lin, S.H. Lee, A. Lambert, Z.Z. Zhao, F. Roseman, Q. Guo, S.D. Gordon, L. Wallace, A.K. Henders, P.M. Visscher, P. Kraft, N.G. Martin, A.P. Morris, S.A. Treloar, S.H. Kennedy, S.A. Missmer, G.W. Montgomery, K.T. Zondervan Genome-wide association study identifies a locus at 7p15.2 associated with endometriosis Nat Genet 43 2011 51 54
5. J.L. Simpson, S. Elias, L.R. Malinak, V.C. Buttram Jr Heritable aspects of endometriosis I. Genetic studies Am J Obstet Gynecol 137 1980 327 331 (Pubitemid 10068718)
6. S.E. Rier, D.C. Martin, R.E. Bowman, W.P. Dmowski, J.L. Becker Endometriosis in rhesus monkeys (Macaca mulatta) following chronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin Fundam Appl Toxicol 21 1993 433 441 (Pubitemid 23338558)
7. D.L. Anger, W.G. Foster The link between environmental toxicant exposure and endometriosis Front Biosci 13 2008 1578 1593 (Pubitemid 351594727)
8. K.M. Zeitoun, S.E. Bulun Aromatase: a key molecule in the pathophysiology of endometriosis and a therapeutic target Fertil Steril 72 1999 961 969
9. H. Cakmak, O. Guzeloglu-Kayisli, U.A. Kayisli, A. Arici Immune-endocrine interactions in endometriosis Front Biosci 1 2009 429 443
10. P.K. Bondza, R. Maheux, A. Akoum Insights into endometriosis-associated endometrial dysfunctions: a review Front Biosci 1 2009 415 428
11. J.A. Sampson Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation Am J Pathol 3 1927 93 110143
12. A. Akoum, A. Lemay, C. Brunet, J. Hebert Secretion of monocyte chemotactic protein-1 by cytokine-stimulated endometrial cells of women with endometriosis Le Groupe d'Investigation en Gynecologie Fertil Steril 63 1995 322 328
13. A. Akoum, M. Al-Akoum, A. Lemay, R. Maheux, M. Leboeuf Imbalance in the peritoneal levels of interleukin 1 and its decoy inhibitory receptor type II in endometriosis women with infertility and pelvic pain Fertil Steril 89 2008 1618 1624 (Pubitemid 351756501)
14. A. Akoum, A. Lemay, S. McColl, L. Turcot-Lemay, R. Maheux Elevated concentration and biologic activity of monocyte chemotactic protein-1 in the peritoneal fluid of patients with endometriosis Fertil Steril 66 1996 17 23 (Pubitemid 26190015)
15. R. Kats, T. Collette, C.N. Metz, A. Akoum Marked elevation of macrophage migration inhibitory factor in the peritoneal fluid of women with endometriosis Fertil Steril 78 2002 69 76 (Pubitemid 34722673)
16. J.A. Keenan, T.T. Chen, N.L. Chadwell, D.S. Torry, M.R. Caudle IL-1 beta. TNF-alpha, and IL-2 in peritoneal fluid and macrophage-conditioned media of women with endometriosis Am J Reprod Immunol 34 1995 381 385 (Pubitemid 3005647)
17. H. Mori, M. Sawairi, M. Nakagawa, N. Itoh, K. Wada, T. Tamaya Peritoneal fluid interleukin-1 beta and tumor necrosis factor in patients with benign gynecologic disease Am J Reprod Immunol 26 1991 62 67
18. S. Orlando, M. Sironi, G. Bianchi, A.H. Drummond, D. Boraschi, D. Yabes, A. Mantovani Role of metalloproteases in the release of the IL-1 type II decoy receptor J Biol Chem 272 1997 31764 31769 (Pubitemid 28013326)
19. F. Colotta, S.K. Dower, J.E. Sims, A. Mantovani The type II 'decoy' receptor: a novel regulatory pathway for interleukin 1 Immunol Today 15 1994 562 566 (Pubitemid 24353906)
20. P. Bossu, U. Visconti, P. Ruggiero, G. Macchia, M. Muda, R. Bertini, C. Bizzarri, A. Colagrande, V. Sabbatini, G. Maurizi, E. Del Grosso, A. Tagliabue, D. Boraschi Transfected type II interleukin-1 receptor impairs responsiveness of human keratinocytes to interleukin-1 Am J Pathol 147 1995 1852 1861
21. Z. Kondera-Anasz, J. Sikora, A. Mielczarek-Palacz, M. Jonca Concentrations of interleukin (IL)-1alpha. IL-1 soluble receptor type II (IL-1 sRII) and IL-1 receptor antagonist (IL-1 Ra) in the peritoneal fluid and serum of infertile women with endometriosis Eur J Obstet Gynecol Reprod Biol 123 2005 198 203 (Pubitemid 41728366)
22. A. Akoum, C. Lawson, C. Herrmann-Lavoie, R. Maheux Imbalance in the expression of the activating type I and the inhibitory type II interleukin 1 receptors in endometriosis Hum Reprod 22 2007 1464 1473 (Pubitemid 47062820)
23. C. Lawson, N. Bourcier, M. Al-Akoum, R. Maheux, F. Naud, A. Akoum Abnormal interleukin 1 receptor types I and II gene expression in eutopic and ectopic endometrial tissues of women with endometriosis J Reprod Immunol 77 2008 75 84
24. R.W. Noyes, A.T. Hertig, J. Rock Dating the endometrial biopsy Am J Obstet Gynecol 122 1975 262 263
25. S. Defrere, S. Colette, J.C. Lousse, J. Donnez, A. Van Langendonckt Review: luminescence as a tool to assess pelvic endometriosis development in murine models Reprod Sci 16 2009 1117 1124
26. S. Defrere, A. Van Langendonckt, R. Gonzalez Ramos, M. Jouret, M. Mettlen, J. Donnez Quantification of endometriotic lesions in a murine model by fluorimetric and morphometric analyses Hum Reprod 21 2006 810 817 (Pubitemid 43378901)
27. R.J. Wenzl, H. Heinzl Localization of matrix metalloproteinase-2 in uterine endometrium and ectopic implants Gynecol Obstet Invest 45 1998 253 257 (Pubitemid 28241180)
28. H.W. Chung, Y. Wen, S.H. Chun, C. Nezhat, B.H. Woo, M. Lake Polan Matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-3 mRNA expression in ectopic and eutopic endometrium in women with endometriosis: a rationale for endometriotic invasiveness Fertil Steril 75 2001 152 159 (Pubitemid 32041238)
29. H.W. Chung, J.Y. Lee, H.S. Moon, S.E. Hur, M.H. Park, Y. Wen, M.L. Polan Matrix metalloproteinase-2, membranous type 1 matrix metalloproteinase, and tissue inhibitor of metalloproteinase-2 expression in ectopic and eutopic endometrium Fertil Steril 78 2002 787 795
30. C. Bellehumeur, T. Collette, R. Maheux, J. Mailloux, M. Villeneuve, A. Akoum Increased soluble interleukin-1 receptor type II proteolysis in the endometrium of women with endometriosis Hum Reprod 20 2005 1177 1184 (Pubitemid 40790239)
31. J. Donnez, P. Smoes, S. Gillerot, F. Casanas-Roux, M. Nisolle Vascular endothelial growth factor (VEGF) in endometriosis Hum Reprod 13 1998 1686 1690 (Pubitemid 28310515)
32. K.L. Bruner-Tran, E. Eisenberg, G.R. Yeaman, T.A. Anderson, J. McBean, K.G. Osteen Steroid and cytokine regulation of matrix metalloproteinase expression in endometriosis and the establishment of experimental endometriosis in nude mice J Clin Endocrinol Metab 87 2002 4782 4791 (Pubitemid 35247076)
33. J.C. Lousse, S. Defrere, A. Van Langendonckt, J. Gras, R. Gonzalez-Ramos, S. Colette, J. Donnez Iron storage is significantly increased in peritoneal macrophages of endometriosis patients and correlates with iron overload in peritoneal fluid Fertil Steril 91 2009 1668 1675
34. L.L. Hii, P.A. Rogers Endometrial vascular and glandular expression of integrin alpha(v)beta3 in women with and without endometriosis Hum Reprod 13 1998 1030 1035 (Pubitemid 28239216)
35. P.C. Brooks, R.A. Clark, D.A. Cheresh Requirement of vascular integrin alpha v beta 3 for angiogenesis Science 264 1994 569 571
36. M. Adachi, K. Nasu, A. Tsuno, A. Yuge, Y. Kawano, H. Narahara Attachment to extracellular matrices is enhanced in human endometriotic stromal cells: a possible mechanism underlying the pathogenesis of endometriosis Eur J Obstet Gynecol Reprod Biol 155 2011 85 88
37. K.G. Osteen, T.M. Igarashi, G.R. Yeaman, K.L. Bruner-Tran Steroid and cytokine regulation of matrix metalloproteinases and the pathophysiology of endometriosis Gynecol Obstet Invest 57 2004 53 54 (Pubitemid 38186437)
38. J. McLaren, A. Prentice, D.S. Charnock-Jones, S.A. Millican, K.H. Muller, A.M. Sharkey, S.K. Smith Vascular endothelial growth factor is produced by peritoneal fluid macrophages in endometriosis and is regulated by ovarian steroids J Clin Invest 98 1996 482 489 (Pubitemid 26255749)
39. T. Harada, F. Taniguchi, M. Izawa, Y. Ohama, Y. Takenaka, Y. Tagashira, A. Ikeda, A. Watanabe, T. Iwabe, N. Terakawa Apoptosis and endometriosis Front Biosci 12 2007 3140 3151
40. R.N. Taylor, M.D. Mueller Anti-angiogenic treatment of endometriosis: biochemical aspects Gynecol Obstet Invest 57 2004 54 56 (Pubitemid 38186438)
41. H. Fakih, B. Baggett, G. Holtz, K.Y. Tsang, J.C. Lee, H.O. Williamson Interleukin-1: a possible role in the infertility associated with endometriosis Fertil Steril 47 1987 213 217 (Pubitemid 17024497)
42. Y. Taketani, T.M. Kuo, M. Mizuno Comparison of cytokine levels and embryo toxicity in peritoneal fluid in infertile women with untreated or treated endometriosis Am J Obstet Gynecol 167 1992 265 270
43. H. Mori, M. Sawairi, M. Nakagawa, N. Itoh, K. Wada, T. Tamaya Expression of interleukin-1 (IL-1) beta messenger ribonucleic acid (mRNA) and IL-1 receptor antagonist mRNA in peritoneal macrophages from patients with endometriosis Fertil Steril 57 1992 535 542
44. A. Bergqvist, C. Bruse, M. Carlberg, K. Carlstrom Interleukin 1beta, interleukin-6, and tumor necrosis factor-alpha in endometriotic tissue and in endometrium Fertil Steril 75 2001 489 495 (Pubitemid 32175661)
45. A. Akoum, C. Jolicoeur, A. Kharfi, M. Aube Decreased expression of the decoy interleukin-1 receptor type II in human endometriosis Am J Pathol 158 2001 481 489 (Pubitemid 32162166)
46. J.E. Sims, D.E. Smith The IL-1 family: regulators of immunity Nat Rev Immunol 10 2010 89 102
47. M. Sillem, S. Prifti, B. Monga, T. Arslic, B. Runnebaum Integrin-mediated adhesion of uterine endometrial cells from endometriosis patients to extracellular matrix proteins is enhanced by tumor necrosis factor alpha (TNF alpha) and interleukin-1 (IL-1) Eur J Obstet Gynecol Reprod Biol 87 1999 123 127 (Pubitemid 29476528)
48. A. Akoum, A. Lemay, I. Paradis, N. Rheault, R. Maheux Secretion of interleukin-6 by human endometriotic cells and regulation by proinflammatory cytokines and sex steroids Hum Reprod 11 1996 2269 2275 (Pubitemid 26392024)
49. A. Akoum, A. Lemay, C. Brunet, J. Hebert Cytokine-induced secretion of monocyte chemotactic protein-1 by human endometriotic cells in culture The Groupe d'Investigation en Gynecologie Am J Obstet Gynecol 172 1995 594 600
50. A. Akoum, C. Lawson, S. McColl, M. Villeneuve Ectopic endometrial cells express high concentrations of interleukin (IL)-8 in vivo regardless of the menstrual cycle phase and respond to oestradiol by up-regulating IL-1-induced IL-8 expression in vitro Mol Hum Reprod 7 2001 859 866 (Pubitemid 32842754)
51. A. Akoum, A. Lemay, R. Maheux Estradiol and interleukin-1beta exert a synergistic stimulatory effect on the expression of the chemokine regulated upon activation, normal T cell expressed, and secreted in endometriotic cells J Clin Endocrinol Metab 87 2002 5785 5792 (Pubitemid 36034390)
52. D.I. Lebovic, F. Bentzien, V.A. Chao, E.N. Garrett, Y.G. Meng, R.N. Taylor Induction of an angiogenic phenotype in endometriotic stromal cell cultures by interleukin-1beta Mol Hum Reprod 6 2000 269 275 (Pubitemid 30120622)
53. M. Sillem, S. Prifti, A. Koch, M. Neher, J. Jauckus, B. Runnebaum Regulation of matrix metalloproteinases and their inhibitors in uterine endometrial cells of patients with and without endometriosis Eur J Obstet Gynecol Reprod Biol 95 2001 167 174 (Pubitemid 32297710)
54. R.W. Watson, O.D. Rotstein, J. Parodo, R. Bitar, J.C. Marshall The IL-1 beta-converting enzyme (caspase-1) inhibits apoptosis of inflammatory neutrophils through activation of IL-1 beta J Immunol 161 1998 957 962 (Pubitemid 28323562)
55. T. Sunyer, J. Lewis, P. Collin-Osdoby, P. Osdoby Estrogen's bone-protective effects may involve differential IL-1 receptor regulation in human osteoclast-like cells J Clin Invest 103 1999 1409 1418 (Pubitemid 29535497)
56. L.R. Prince, L. Allen, E.C. Jones, P.G. Hellewell, S.K. Dower, M.K. Whyte, I. Sabroe The role of interleukin-1beta in direct and toll-like receptor 4-mediated neutrophil activation and survival Am J Pathol 165 2004 1819 1826 (Pubitemid 39435179)
57. T. Simonart, J.P. Van Vooren Interleukin-1 beta increases the BCL-2/BAX ratio in Kaposi's sarcoma cells Cytokine 19 2002 259 266 (Pubitemid 35352165)
58. K. Kuhn, S. Hashimoto, M. Lotz IL-1 beta protects human chondrocytes from CD95-induced apoptosis J Immunol 164 2000 2233 2239 (Pubitemid 30108784)
59. W. Budzynski, C. Radzikowski Cytotoxic cells in immunodeficient athymic mice Immunopharmacol Immunotoxicol 16 1994 319 346 (Pubitemid 24285733)
60. U.A. Kayisli, M. Berkkanoglu, L. Zhang, G. Kizilay, A. Arici The broad-spectrum chemokine inhibitor NR58-3.14.3 suppresses the implantation and survival of human endometrial implants in the nude mice endometriosis model Reprod Sci 14 2007 825 835 (Pubitemid 351903558)
61. P. Adamson Therapeutic strategies targeting interleukin-1 in vascular inflammation Drug Discov Today 3 2006 367 373 (Pubitemid 44780670)
62. N. Bessis, L. Guery, A. Mantovani, A. Vecchi, J.E. Sims, D. Fradelizi, M.C. Boissier The type II decoy receptor of IL-1 inhibits murine collagen-induced arthritis Eur J Immunol 30 2000 867 875 (Pubitemid 30216260)
63. A. Jager, D. Zhang, A. Kawarizadeh, R. Tolba, B. Braumann, S. Lossdorfer, W. Gotz Soluble cytokine receptor treatment in experimental orthodontic tooth movement in the rat Eur J Orthod 27 2005 1 11 (Pubitemid 41219065)
64. T.M. D'Hooghe, C.M. Kyama, D. Chai, A. Fassbender, A. Vodolazkaia, A. Bokor, J.M. Mwenda Nonhuman primate models for translational research in endometriosis Reprod Sci 16 2009 152 161